Abstract

Predation exerts one of the greatest selective pressures on prey organisms. Many studies showed the existence of innate anti-predator responses mostly in early stages of juveniles vertebrate. Learning is also possible but risky since it can cause death. There is now growing evidence that embryonic learning exists in animals but few studies have tested explicitly for learning in embryos. Here, Sepia pharaonis cuttlefish embryos respond to the presence or odour of a predator fish but not to a non-predator fish. Interestingly, embryos can learn to associate a non-threatening stimulus with an alarm signal: cuttlefish ink. After several paired exposures, they respond to the harmless fish as if it were dangerous. Our results demonstrate both innate and acquired predator recognition in a cephalopod. Embryos response is a decrease of ventilation rate. Such response is adaptive, especially in a translucent egg, since it reduces movement and hence the risk of being detected; this freezing-like behaviour may also reduce bioelectric field, which lessens shark predation risk. Last, our result is the first report of associative learning in an invertebrate embryo. This shows that a cuttlefish embryo can have both genetic predator avoidance skills and possesses enough cognitive abilities plasticity to learn and retain new threats before hatching. The combination of these mechanisms is an impressive example of the early adaptability of cephalopod molluscs. This amount of behavioural plasticity gives the newly-hatched sepia a huge selective advantage when dealing with known or new threats.

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